Yale Research Advances Understanding of Biosolids Pathogen Risk

In recent years, Dr. Jordan Peccia’s research group at Yale University has been one of several focusing on pathogens in biosolids land application systems.  In June 2011, a paper from the Peccia group was published in Environmental Science & Technology (ES&T).

In recent years, Dr. Jordan Peccia’s research group at Yale University has been one of several focusing on pathogens in biosolids land application systems.  In June 2011, a paper from the Peccia group was published in Environmental Science & Technology (ES&T). The lead author was Emily Viau, who completed her PhD from Yale this spring.  It presented an updated quantitative microbial risk analysis (QMRA) of the potential for human infection from airborne pathogens resulting from Class B land application – most particularly from the time-limited events of loading biosolids into spreaders and spreading them. ES&T printed a parallel summary article that created some concerns in the biosolids profession because of its increased emphasis on the potential risk from, in particular, norovirus in biosolids.

Dr. Peccia completed graduate work in environmental engineering, focused first on the fate of hydrocarbons in soil and then on bioaerosols.  He then was an assistant professor at Arizona State University, where he conducted biosolids bioaerosol field studies.  (Nearby at the University of Arizona, Brooks, Pepper, and Gerba have conducted similar research.)

Now at Yale, Dr. Peccia and several students have been working further on understanding the potential risks from bioaerosols emitted during land application of Class B biosolids.  Research indicates that bioaerosols present the greatest potential risk of human infection from Class B biosolids applications, with the exception of accidental direct ingestion of Class B biosolids.

A late June 2011 phone discussion with Dr. Peccia provided clarification on the significance of his group’s latest findings and publication.

The first thing Dr. Peccia noted is that he thought the author of the ES & T summary article tried to derive overly clear-cut conclusions from the Viau et al. (2011) paper.  In such a complex topic, it is rare that a single paper is a major game-changer.   Dr. Peccia’s group has published several papers leading up to the current one, and they incorporated many others’ findings into their current risk analysis as well.  The current paper is a synthesis, attempting to reach some consensus on the known risks – and less-well-known risks – from Class B biosolids pathogens.

What their new risk analysis confirmed – consistent with others’ analyses – is that, for the better-understood and easier-to-measure pathogens, the risk of infection is low:  “independent results from different models do result in similar risk estimations near 10--4 for enterovirus.”  However, the first key take-home message is “that risk analysis must be expanded to include additional, more relevant pathogens….”

In particular, Viau et al. notes that it seems that noroviruses (Norwalk-like viruses) are less-well understood and appear to possibly present a higher level of risk than enterovirus and Salmonella.  Because these viruses cannot be cultured, identification and enumeration became easier only in the 1990s, when polymerase chain reaction (PCR) methods became widely used. According to Dr. Peccia, previous work by his group and by Calvin Wong when he was at Michigan State and by the University of Arizona researchers have identified norovirus in Class B biosolids, apparently in fairly significant numbers, because even relatively crude tests found it.  Noroviruses seem to be resistant to at least some Class B treatments (Dr. Peccia’s group has focused its work on mesophilic anaerobically digested biosolids).

Noroviruses are the leading cause of gastrointestinal illness and are transmitted generally by fecal-oral exposure.  However, there is documentation of infection via airborne norovirus, which requires inhalation of the virus particles, which get trapped in airway cilia and are then ingested by swallowing.  This route of exposure makes for a low percentage of virus reaching the digestive tract, something that Dr. Peccia’s group had to consider in their risk analysis (they assumed a lower rate of ingestion by this route than used in some previous risk analyses).

Viau et al. emphasizes the limits of modeling and risk analysis: “the uncertainty in estimating risk must be evaluated in all risk-based results.”  This leads to the second key take-home message, which the authors even included in the abstract: “Quantitative microbial risk assessment for biosolids exposure more effectively operates as a tool for analyzing how exposure can be reduced rather than being used to assess ‘safety.’”  Thus, any claims that this paper indicates that Class B biosolids land application is either safe or unsafe are misinterpretations.  Complex science is not black and white.  Scientists hedge, especially when modeling with significant levels of uncertainty.  The value of this kind of work is to get a general sense of whether or not something might present enough of a risk to warrant further research.

In addition, modeling and risk analysis cannot be viewed alone; they must be compared to other similar risks and field observations.  Dr. Peccia’s group has done some past research comparing pathogens in manures and soils, as well as biosolids.  And their work leading up to the current risk analysis includes several studies in the field at live land application sites.  Still, one has to ask if the Viau et al. estimate of a 10 -2 annual probability of infection from norovirus makes sense.  Are there 1 in 100 people adjacent to land application sites showing this kind of gastrointestinal infection?  Because norovirus is the most common cause of gastrointestinal distress in the U. S., it becomes more difficult to be sure where any particular infection comes from.

Which leads to the third key message from the Viau et al. paper: the challenge of using epidemiology to evaluate Class B biosolids land application.  As Dr. Peccia explained, for epidemiology to accurately determine an actual rate of impact of something, the test population has to be considerably larger than the probability estimate:  “studies that enroll less than 1000 subjects may not be able to identify statistically relevant health effects unless the risk is very high (greater than 1 in 100 probability of illness). Even then, several more independent studies are needed to form any actionable conclusion.”

There have been only a few attempts at epidemiological evaluation of Class B biosolids land application, and, as Viau et al. note, “the limited past studies serve only to demonstrate and foster uncertainty about biosolids health effects.”  Viau et al. cite the most comprehensive epidemiological  study, conducted in Ohio and published in 1985 (Dorn et al.), “which demonstrated no greater incidence of adverse health effects over control groups located away from land application sites.”  But they then cite a study in Ohio (Khuder et al., 2007) that relied on self-reporting; that study’s findings seemed to imply significant risks to neighbors of land application sites.  But they were inconclusive and unreliable, as its authors eventually noted, because of the many assumptions and uncertainties the research contained, as well as the self-reported nature of the complaints (contact NEBRA for copies of this work and a 2008 WEA of Ohio review).

So, the fact is that epidemiological research on this topic seems unlikely to find anything conclusive – especially to skeptics. This leaves only investigation of self-reported impacts and similar less-robust surveying (as in Khuder et al., 2007) as the only tools for attempting to independently validate risk modeling and analysis.

This is why Viau et al. and other researchers are counting on quantitative microbial risk analysis (QMRA) as the best scientific tool available.  Viau et al. note that there have been eight such QMRAs.  The difference with theirs is that enough data has accumulated to begin to analyze not just for Salmonella and enteroviruses and other traditional indicator pathogens, but also adenoviruses and noroviruses.

So the science and research is expanding properly, reaching to utilize new technologies for detecting, enumerating, and understanding pathogens that have not been looked at so closely yet.  But, as Dr. Peccia confirmed, this one step they have taken in advancing the science only suggests the need for more research – especially on noroviruses – and does not suggest any need for dramatic changes in current practices.

Still, Dr. Peccia notes, in their recent paper, the team also chose to emphasize that risk analysis can help to identify ways for reducing risks.  The fourth and final take-home message he emphasized is that reducing pathogens in biosolids through advanced (e.g. Class A) treatments is far more effective at reducing potential risks to neighbors of land application sites than increasing set-back distances (although increasing set-back distances does reduce risk some).

Dr. Peccia hopes that more research will be done on noroviruses and adenoviruses.  He thinks EPA should get a ““better picture of all pathogens in order to ensure their regulations are effective.” And he encourages follow-up with anyone reporting illness that they think may be associated with Class B biosolids.  While in most cases, it is impossible to make any causal connection, doing such follow-up may be the only way to get some sense of whether the modeled and estimated risks from these less-well-understood pathogens are accurate or not.

The recent Viau et al. paper from Dr. Peccia’s group at Yale will likely and appropriately spur more attention on some of these lesser-known pathogens.  However, it is important to remember, that, just as with traces of personal care products that are found in biosolids, these pathogens are not new in Class B biosolids – we’re just able to measure their presence and fate more than before.    With thousands of biosolids land application events happening every year going back decades, it seems obvious that, if these pathogens did present a significant and unacceptably high risk to biosolids land appliers, farmers, and neighbors, there would be significant evidence, especially, perhaps, of gastrointestinal distress from norovirus.  Yet the self-reported symptoms catalogued by Harrison and Oakes (2002) of Cornell Waste Management Institute and Lewis and Gattie (2002) of University of Georgia are more respiratory in nature.

And what does this mean for the biosolids manager?

First, it seems certain that Class A treatment does reduce pathogen risks considerably further.  Whether or not such a reduction is necessary depends on the local situation and management techniques.  Class B biosolids can provide greater fertilizer benefits to farmers, and these benefits must be weighed against potential risks.

Second, following regulations and best management practices for Class B biosolids land application is important – they reduce risks!  In 2002, the CDC/NIOSH created ”Guidance on Controlling Potential Risks to Workers Exposed to Class B Biosolids” that advised basic hygiene precautions to reduce risks from pathogens – washing hands, avoiding ingestion, not smoking and eating during biosolids work, and avoiding inhalation of dust and aerosols.  Following these guidelines should be effective against any biosolids pathogens, including norovirus.

The recent work of Dr. Peccia’s group at Yale seems to corroborate – and further advance - understanding of risks from Class B biosolids.  The state of understanding was summarized by Commonwealth of Virginia epidemiologists’ review (Jenkins et al., 2007):

“Research is constantly contributing information to provide the missing data and help formulate standards to reduce risk, but it must be remembered that as long as sewage is produced, it is not possible to have a totally risk-free environment. Every method of sewage disposal contains health and environmental risks. The goal is to reduce the risks as much as possible, be able to quantify those risks, and then balance the level of risk against the cost of risk reduction, against competing risks, and/or against risk generally accepted as trivial or acceptable. The end product of a risk-based approach either identifies an acceptable level of exposure or prescribes technical controls or political processes needed to attain acceptable risk. Despite all the data gaps and concerns about the basis for developing the 503 rule, the NRC Committee [2002 National Research Council report] did not recommend eliminating the application of biosolids to land.

“Although much still needs to be learned about the content, bioavailability and fate of chemicals and pathogens in biosolids and their health effects, there does not seem to be strong evidence of serious health risks when biosolids are managed and monitored appropriately. Human health allegations associated with biosolids usually lack evidence of biological absorption, medically determined human health effects, and/or do not meet the biological plausibility test. On the other hand, no concerted effort has been made to collect and analyze data on reported health effects resulting from biosolids applied to land. [This is being addressed by a Water Environment Research Foundation study.]

“To protect the public and ensure public confidence in the system, it is incumbent upon regulatory bodies to ensure that all standards are based on the best available science and that recommendations are assiduously applied. This includes updating the riskassessment methods used for chemical contaminants and incorporating risk assessment methodology in the evaluation of health risks from pathogens.”

Which is exactly what Dr. Peccia’s group at Yale is doing. Their research is summarized here. (http://www.eng.yale.edu/peccialab/research_biosolids.html).



Dorn, C.; Reddy, C.; Lamphere, D.; Gaeuman, J.; Lanese, R.  Municipal Sewage Sludge Application on Ohio Farms: Health Effects. Environ. Res. 1985, 38, 332–359.

Harrison, E.; Oaks, S. R. Investigation of alleged health incidents associated with land application of sewage sludges. New Solutions 2002,12, 387–408.

Jenkins, S. R.; C.W. Armstrong; and M. M. Monti. 2007.  Health Effects of Biosolids Applied to Land: Available Scientific Evidence.. Available at www.vdh.state.va.us/epidemiology/DEE/documents/Biosolidsfinal.pdf

Lewis, D. L.; Gattie, D. K. Pathogen risks from applying sewage sludge to land. Environ. Sci. Technol. 2002, 36, 286A–293A.

Viau, E.; K. Bibby, T. Paez-Rubio; and J. Peccia.  2011. Toward a Consensus View on the Infectious Risks Associated with Land Application of Sewage Sludge.  Environ. Sci. Technol., 2011, 45 (13), pp 5459–5469